Selective recruitment of NAT10-catalyzed ac4C-modified mRNAs into stress granules by poly(A)-binding protein promotes mRNA stability and plant heat stress tolerance.

Abstract

Global warming poses a considerable threat to crop production, making heat stress a pivotal challenge in agriculture. Yet how epitranscriptomic modifications contribute to plant heat stress responses remains to be explored. Here, this study reveals the critical role of phase separation in plant heat stress tolerance and demonstrated that N-acetyltransferase 10 (NAT10), which encodes of the cytosine N4 acetyltransferase protein, contributes to heat resistance. We found that NAT10 interacts with polyadenylate-binding protein (PABP), which contains intrinsically disordered regions (IDRs), thereby facilitating the selective recruitment of ac4C-modified mRNAs into PABP-mediated condensates. Integrative transcriptome-wide analysis, combining ac4C acetylome profiling with SG-enriched transcript sequencing, revealed that detoxification-related mRNAs, including those encoding the cytochrome P450, phenylalanine ammonia-lyase, glutathione S-transferase, and heat shock 70 protein families, preferentially accumulate within these condensates. This accumulation maintains their stability and prevents stress-induced degradation. Conversely, loss of PABP impairs the recruitment of ac4C-modified detoxification-related transcripts into stress granules, thereby promoting their degradation under heat stress. In summary, our findings identify a stress-responsive NAT10-PABP-ac4C axis that promotes phase separation to stabilize ac4C-modified mRNAs under heat stress. By recruiting detoxification-related transcripts into stress granules, this axis ensures mRNA stability and offers insights for enhancing crop resilience under environmental stress.